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Native Lespedeza species harbor greater non-rhizobial bacterial diversity in root nodules compared to the coexisting invader, L. cuneata

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Abstract

Background and Aims

Lespedeza cuneata is a non-native invasive legume that alters the soil bacterial community, associates promiscuously with rhizobia, and benefits more from rhizobial interactions compared to coexisting native Lespedeza in North America. We tested the hypothesis that native congeners differ in their nodule bacteria associations compared to L. cuneata.

Methods

Plots with high L. cuneata invasion, low L. cuneata invasion with native Lespedeza species present, and uninvaded plots where native Lespedeza species existed without L. cuneata were sampled. Nodules were collected from all Lespedeza species present, and Chamaecrista fasciculata, a common native annual legume. Bacterial DNA from nodules was isolated and sequenced.

Results

Nodule bacterial composition differed significantly between hosts. L. cuneata nodules contained high frequencies of rhizobial DNA and low bacterial diversity, while native Lespedeza nodules contained lower rhizobial frequencies and higher non-rhizobial bacterial diversity. Specific non-rhizobial bacterial groups exhibited strong associations with native legumes and uninvaded sites.

Conclusions

Significant differences exist in the nodule bacterial composition between native legumes and an introduced congener. The mechanism(s) and ecological importance of these differences remain unknown. These differences in bacterial associations could influence not only the competitive ability of the invader, but recovery of invaded sites as well.

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References

  • Annapurna K, Ramadoss D, Bose P, VithalKumar L (2013) In situ localization of Paenibacillus polymyxa HKA-15 in roots and root nodules of soybean (Glycine max. L.). Plant Soil 373:641–648

    Article  CAS  Google Scholar 

  • Aserse AA, Räsänen LA, Aseffa F, Hailemariam A, Lindström K (2013) Diversity and sporadic symbionts and nonsymbiotic endophytic bacteria isolated from nodules of woody, shrub, and food legumes in Ethiopia. Appl Microbiol Biot 97:10117–10134

    Article  CAS  Google Scholar 

  • Bai Y, D’Aoust F, Smith DL, Driscoll BT (2002) Isolation of plant-growth-promoting Bacillus strains from soybean root nodules. Can J Microbiol 48:230–238

    Article  CAS  PubMed  Google Scholar 

  • Bai Y, Zhou X, Smith DL (2003) Enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43:1774–1781

    Article  Google Scholar 

  • Baldwin JG, Barker KR, Nelson LA (1979) Effect of Meloidogyne incognita on nitrogen fixation in soybean. J Nematol 11:156–161

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boukhatem AF, Domergue O, Bekki A, Merabet C, Sekkour S, Bouazza F, Duponnois R, de Lajudie P, Galiana A (2012) Symbiotic characterization and diversity of rhizobia associated with native and introduced acacias in arid and semi-arid regions of Algeria. FEMS Microbiol Ecol 80:534–547

    Article  CAS  PubMed  Google Scholar 

  • Burke JM, Miller JE, Mosjidis JA, Terrill TH (2012) Grazing sericea lespedeza for control of gastrointestinal nematodes in lambs. Vet Parasitol 186:507–512

    Article  CAS  PubMed  Google Scholar 

  • Callaway RM, Bedmar EJ, Reinhart KO, Silvan CG, Klironomos J (2011) Effects of soil biota from different ranges on Robinia invasion: acquiring mutualists and escaping pathogens. Ecology 92:1027–1035

    Article  PubMed  Google Scholar 

  • Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733

    Article  CAS  PubMed  Google Scholar 

  • Dudeja SS, Giri R, Saini R, Suneja-Madan P, Kothe E (2012) Interaction of endophytic microbes with legumes. J Basic Microb 52:248–260

    Article  CAS  Google Scholar 

  • Erdman LW (1950) The effectivity of different strains of Rhizobium on annual and perennial lespedezas. Soil Sci Soc Am Pro 15:173–176

    Article  Google Scholar 

  • Gu CT, Wang ET, Sui XH, Chen WF, Chen WX (2007) Diversity and geographical distribution of rhizobia associated with Lespedeza spp. in temperate and subtropical regions of China. Arch Microbiol 188:355–365

    Article  CAS  PubMed  Google Scholar 

  • Horiuchi J, Prithiviraj B, Bais HP, Kimball BA, Vivanco JM (2005) Soil nematodes mediate positive interactions between legume plants and rhizobium bacteria. Planta 222:848–857

    Article  CAS  PubMed  Google Scholar 

  • Hu L, Busby RR, Gebhart DL, Yannarell AC (2014) Invasive Lespedeza cuneata and native Lespedeza virginica experience asymmetrical benefits from rhizobial symbionts. Plant Soil 384:315–325

    Article  CAS  Google Scholar 

  • Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319

    Article  CAS  PubMed  Google Scholar 

  • Hung PQ, Kumar SM, Govindsamy V, Annapurna K (2007) Isolation and characterization of endophytic bacteria from wild and cultivated soybean varieties. Biol Fert Soils 44:155–162

    Article  Google Scholar 

  • Hungria M, Nogueira MA, Araujo RS (2013) Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability. Biol Fert Soils 49:791–801

    Article  Google Scholar 

  • Ibáñez F, Angelini J, Taurian T, Tonelli ML, Fabra A (2009) Endophytic occupation of peanut root nodules by opportunistic Gammaproteobacteria. Syst Appl Microbiol 32:49–55

    Article  PubMed  Google Scholar 

  • Ibewiro B, Sanginga N, Vanlauwe B, Merckx R (2000) Influence of phytoparasitic nematodes on symbiotic N2 fixation in tropical herbaceous legume cover crops. Biol Fert Soils 31:254–260

    Article  CAS  Google Scholar 

  • Kardol P, Cregger MA, Campany CE, Classen AT (2010) Soil ecosystem functioning under climate change: plant species and community effects. Ecology 91:767–781

    Article  PubMed  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Kommuru DS, Barker T, Desai S, Burke JM, Ramsay A, Mueller-Harvey I, Miller JE, Mosjidis JS, Kamisetti N, Terrill TH (2014) Use of pelleted sericea lespedeza (Lespedeza cuneata) for natural control of coccidian and gastrointestinal nematodes in weaned goats. Vet Parasitol 204:191–198

    Article  CAS  PubMed  Google Scholar 

  • Kumar V, Pathak CV, Dudeja SS, Saini R, Giri R, Narula S, Anand RC (2013) Legume nodule endophytes more diverse than endophytes from roots of legumes or non legumes in soils of Haryana, India. J Microbiol Biotechnol Res 3:83–92

    Google Scholar 

  • Lei X, Wang ET, Chen WF, Sui XH, Chen WX (2008) Diverse bacteria isolated from root nodules of wild Vicia species grown in temperate region of China. Arch Microbiol 190:657–671

    Article  CAS  PubMed  Google Scholar 

  • Leyns F, De Cleene M, Swings JG, De Ley J (1984) The host range of the genus Xanthomonas. Bot Rev 50:308–356

    Article  Google Scholar 

  • Mishra PK, Mishra S, Selvakumar G, Kundu S, Gupta HS (2009) Enhanced soybean (Glycine max L.) plant growth and nodulation by Bradyrhizobium japonicum-SB1 in presence of Bacillus thuringiensis-KR1. Acta Agric Scand Sect B Soil Plant Sci 59:189–196

    CAS  Google Scholar 

  • Naisbitt T, James EK, Sprent JL (1992) The evolutionary significance of the legume genus Chamaechrista, as determined by nodule structure. New Phytol 122:487–492

    Article  Google Scholar 

  • Palaniappan P, Chauhan PS, Saravanan VS, Anandham R, Sa T (2010) Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biol Fert Soils 46:807–816

    Article  Google Scholar 

  • Pandya M, Kumar GN, Rajkumar S (2013) Invasion of rhizobial infection thread by non-rhizobia for colonization of Vigna radiata root nodules. FEMS Microbiol Lett 348:58–65

    Article  CAS  PubMed  Google Scholar 

  • Parker MA (2001) Mutualism as a constraint on invasion success for legumes and rhizobia. Divers Distrib 7:125–136

    Article  Google Scholar 

  • Parker MA, Malek W, Parker IM (2006) Growth of an invasive legume is symbiont limited in newly occupied habitats. Divers Distrib 12:563–571

    Article  Google Scholar 

  • Parker MA, Wurtz AK, Paynter Q (2007) Nodule symbiosis of invasive Mimosa pigra in Australia and in ancestral habitats: a comparative analysis. Biol Invasions 9:127–138

    Article  Google Scholar 

  • Pérez-Fernández MA, Lamont BB (2003) Nodulation and performance of exotic and native legumes in Australian soils. Aust J Bot 51:543–553

    Article  Google Scholar 

  • Peterson AT, Papes M, Kluze DA (2003) Predicting the potential invasive distributions of four alien plant species in North America. Weed Sci 51:863–868

    Article  CAS  Google Scholar 

  • van der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1:28–37

    Article  PubMed  Google Scholar 

  • Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457

    Article  PubMed  Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmánek M (2000) Plant invasions- the role of mutualisms. Biol Rev 75:65–93

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Echeverría S, Crisóstomo JA, Nabais C, Freitas H (2009) Belowground mutualists and the invasive ability of Acacia longifolia in coastal dunes of Portugal. Biol Invasions 11:651–661

    Article  Google Scholar 

  • Ródriguez-Echeverría S, Fajardo S, Ruiz-Díez B, Fernández-Pascual M (2012) Differential effectiveness of novel and old legume-rhizobia mutualisms: implications for invasion by exotic legumes. Oecologia 170:253–261

    Article  PubMed  Google Scholar 

  • Selvakumar G, Kundu S, Gupta AD, Shouche YS, Gupta HS (2008) Isolation and characterization of nonrhizobial plant growth promoting bacteria from nodules of kudzu (Pueraria thunbergiana) and their effect on wheat seedling growth. Curr Microbiol 56:134–139

    Article  CAS  PubMed  Google Scholar 

  • Selvakumar G, Panneerselvam P, Ganeshamurthy AN (2013) Legume root nodule associated bacteria. In: Aurora NK (ed) Plant microbe symbiosis: fundamentals and advances. Springer, New Delhi, pp. 215–232

    Chapter  Google Scholar 

  • Sprent JI (2001) Nodulation in legumes. Royal Botanic Gardens, London

    Google Scholar 

  • Sturz AV, Christie BR, Matheson BG, Nowak J (1997) Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biol Fert Soils 25:13–19

    Article  Google Scholar 

  • Talbot G, Topp E, Palin MF, Massé DI (2008) Evaluation of molecular methods used for establishing the interactions and functions of microorganisms in anaerobic bioreactors. Water Res 42:513–537

    Article  CAS  PubMed  Google Scholar 

  • Tang J, Bromfield ESP, Rodrigue N, Cloutier S, Tambong JT (2012) Microevolution of symbiotic Bradyrhizobium populations associated with soybeans in east North America. Ecol Evol 2:2943–2961

    Article  PubMed  PubMed Central  Google Scholar 

  • Tariq M, Hameed S, Yasmeen T, Ali A (2012) Non-rhizobial bacteria for improved nodulation and grain yield of mung bean [Vigna radiata (L.) Wilczek]. Afr J Biotechn 11:15012–15019

    CAS  Google Scholar 

  • Tariq M, Hameed S, Yasmeen T, Zahid M, Zafar M (2014) Molecular characterization and identification of plant growth promoting endophytic bacteria isolated from the root nodules of pea (Pisum sativum L.). World J Microb Biot 30:719–725

    Article  CAS  Google Scholar 

  • Taurian T, Ibanéz F, Angelini J, Tonelli ML, Fabra A (2012) Endophytic bacteria and their role in legumes growth promotion. In: Maheshwari DK (ed) Bacteria in agrobiology: plant probiotics. Springer-Verlag, Berlin, pp. 141–168

    Chapter  Google Scholar 

  • Trujillo ME, Alonso-Vega P, Rodríguez R, Carro L, Cerda E, Alonso P, Martínez-Molina E (2010) The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius. ISME J 4:1265–1281

    Article  PubMed  Google Scholar 

  • Tye DRC, Drake DC (2012) An exotic Australian Acacia fixes more N than a coexisting indigenous Acacia in South African riparian zone. Plant Ecol 213:251–257

    Article  Google Scholar 

  • Velázquez E, Martínez-Hidalgo P, Carro L, Alonso P, Peix Á, Trujillo M, Martínez-Molina E (2014) Nodular endophytes: an untapped diversity. In: González MBR, Gonzalez-López J (eds) Beneficial plant-microbial interactions: ecology and applications. CRC Press, Boca Raton, pp. 215–236

    Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Microbiol Biot 73:5261–5267

    CAS  Google Scholar 

  • Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477–487

    Article  Google Scholar 

  • Yannarell AC, Busby RR, Denight ML, Gebhart DL, Taylor SJ (2011) Soil bacteria and fungi respond on different spatial scales to invasion by the legume Lespedeza cuneata. Front Microbiol 2:127. doi:10.3389/fmicb.2011.00127

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This research was funded by the United States Army A896 Direct Funded Research Program.

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Authors and Affiliations

  1. U.S. Army Engineer Research and Development Center, 2902 Newmark Drive, Champaign, IL, 61822, USA

    Ryan R. Busby, Giselle Rodriguez & Dick L. Gebhart

  2. Department of Natural Resources and Environmental Sciences, University of Illinois, 1102 South Goodwin Avenue, Urbana, IL, 61801, USA

    Anthony C. Yannarell

Authors
  1. Ryan R. Busby
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  2. Giselle Rodriguez
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  3. Dick L. Gebhart
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  4. Anthony C. Yannarell
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Correspondence to Ryan R. Busby.

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Responsible Editor: Katharina Pawlowski.

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Busby, R.R., Rodriguez, G., Gebhart, D.L. et al. Native Lespedeza species harbor greater non-rhizobial bacterial diversity in root nodules compared to the coexisting invader, L. cuneata . Plant Soil 401, 427–436 (2016). https://doi.org/10.1007/s11104-015-2763-3

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